The azimuthal path of myosin V and its dependence on lever-arm length

Journal of General Physiology

Volumn 139, Issue 2, 2012, Pages 101-120

  Lewis, John H ^a   Beausang, John F ^a   Sweeney, H Lee ^a   Goldman, Yale E ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; HYBRID PROTEIN; MOLECULAR MOTOR; MYOSIN V;

ANIMAL; ARTICLE; CHEMISTRY; CHICKEN; FLUORESCENCE POLARIZATION; METABOLISM; METHODOLOGY; POLARIZATION MICROSCOPY; PROTEIN TERTIARY STRUCTURE; RABBIT; STRUCTURE ACTIVITY RELATION;

ACTINS; ANIMALS; CHICKENS; FLUORESCENCE POLARIZATION; MICROSCOPY, POLARIZATION; MOLECULAR MOTOR PROTEINS; MYOSIN TYPE V; PROTEIN STRUCTURE, TERTIARY; RABBITS; RECOMBINANT FUSION PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84863393705     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201110715     Document Type: Article

References (49)

1. Ali, M.Y., S. Uemura, K. Adachi, H. Itoh, K. Kinosita Jr., and S. Ishiwata. 2002. Myosin V is a left-handed spiral motor on the right-handed actin helix. Nat. Struct. Biol. 9:464-467. http://dx.doi.org/10.1038/nsb803.
2. Ali, M.Y., E.B. Krementsova, G.G. Kennedy, R. Mahaffy, T.D. Pollard, K.M. Trybus, and D.M. Warshaw. 2007. Myosin Va maneuvers through actin intersections and diffuses along microtubules. Proc. Natl. Acad. Sci. USA. 104:4332-4336. http://dx.doi.org/10.1073/pnas.0611471104.
3. Amos, L.A., and W.B. Amos. 1991. Molecules of the Cytoskeleton. Guilford Press. 253 pp.
4. Beausang, J.F., H.W. Schroeder III, P.C. Nelson, and Y.E. Goldman. 2008a. Twirling of actin by myosins II and V observed via polarized TIRF in a modified gliding assay. Biophys. J. 95:5820-5831. http://dx.doi.org/10.1529/biophysj.108.140319.
5. Beausang, J.F., Y. Sun, and Y.E. Goldman. 2008b. Single molecule fluorescence polarization via polarized total internal reflection fluorescent microscopy. In Laboratory Manual for Single Molecule Studies. P.R. Selvin and T.J. Ha, editors. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 121-148.
6. Block, S.M. 2007. Kinesin motor mechanics: binding, stepping, tracking, gating, and limping. Biophys. J. 92:2986-2995. http://dx.doi.org/10.1529/biophysj.106.100677.
7. Bustamante, C., W. Cheng, and Y.X. Mejia. 2011. Revisiting the central dogma one molecule at a time. Cell. 144:480-497. http://dx.doi.org/10.1016/j.cell.2011.01.033.
8. Cheney, R.E., M.K. O'Shea, J.E. Heuser, M.V. Coelho, J.S. Wolenski, E.M. Espreafico, P. Forscher, R.E. Larson, and M.S. Mooseker. 1993. Brain myosin-V is a two-headed unconventional myosin with motor activity. Cell. 75:13-23.
9. Cooke, R. 1986. The mechanism of muscle contraction. CRC Crit. Rev. Biochem. 21:53-118. http://dx.doi.org/10.3109/10409238609113609.
10. Corrie, J.E., and J.S. Craik. 1994. Synthesis and characterization of iodacetamidotetramethylrhodamine. J. Chem. Soc. Perkin Trans.1: 2967-2973. http://dx.doi.org/10.1039/p19940002967.
11. Corrie, J.E., J.S. Craik, and V.R. Munasinghe. 1998. A homobifunctional rhodamine for labeling proteins with defined orientations of a fluorophore. Bioconjug. Chem. 9:160-167. http://dx.doi.org/ 10.1021/bc970174e.
12. Corrie, J.E., B.D. Brandmeier, R.E. Ferguson, D.R. Trentham, J. Kendrick-Jones, S.C. Hopkins, U.A. van der Heide, Y.E. Goldman, C. Sabido-David, R.E. Dale, et al. 1999. Dynamic measurement of myosin light-chain-domain tilt and twist in muscle contraction. Nature. 400:425-430. http://dx.doi.org/10.1038/22704.
13. Dobbie, I., M. Linari, G. Piazzesi, M. Reconditi, N. Koubassova, M.A. Ferenczi, V. Lombardi, and M. Irving. 1998. Elastic bending and active tilting of myosin heads during muscle contraction. Nature. 396:383-387. http://dx.doi.org/10.1038/24647.
14. Egelman, E.H. 1997. New angles on actin dynamics. Structure. 5:1135-1137. http://dx.doi.org/10.1016/S0969-2126(97)00264-5.
15. Endow, S.A., and H. Higuchi. 2000. A mutant of the motor protein kinesin that moves in both directions on microtubules. Nature. 406:913-916. http://dx.doi.org/10.1038/35022617.
16. Forkey, J.N., M.E. Quinlan, and Y.E. Goldman. 2000. Protein structural dynamics by single-molecule fluorescence polarization. Prog. Biophys. Mol. Biol. 74:1-35. http://dx.doi.org/10.1016/S0079-6107(00)00015-8.
17. Forkey, J.N., M.E. Quinlan, M.A. Shaw, J.E. Corrie, and Y.E. Goldman. 2003. Three-dimensional structural dynamics of myosin V by singlemolecule fluorescence polarization. Nature. 422:399-404. http:// dx.doi.org/10.1038/nature01529.
18. Forkey, J.N., M.E. Quinlan, and Y.E. Goldman. 2005. Measurement of single macromolecule orientation by total internal reflection fluorescence polarization microscopy. Biophys. J. 89:1261-1271. http://dx.doi.org/10.1529/biophysj.104.053470.
19. Gennerich, A., and R.D. Vale. 2009. Walking the walk: how kinesin and dynein coordinate their steps. Curr. Opin. Cell Biol. 21:59-67. http://dx.doi.org/10.1016/j.ceb.2008.12.002.
20. Hecht, E. 2001. Optics. Fourth edition. Addison Wesley, New York. 680 pp.
21. Klostermeier, D. 2011. Single-molecule FRET reveals nucleotidedriven conformational changes in molecular machines and their link to RNA unwinding and DNA supercoiling. Biochem. Soc. Trans. 39:611-616. http://dx.doi.org/10.1042/BST0390611.
22. Kodera, N., D. Yamamoto, R. Ishikawa, and T. Ando. 2010. Video imaging of walking myosin V by high-speed atomic force microscopy. Nature. 468:72-76. http://dx.doi.org/10.1038/nature09450.
23. Mehta, A.D., R.S. Rock, M. Rief, J.A. Spudich, M.S. Mooseker, and R.E. Cheney. 1999. Myosin-V is a processive actin-based motor. Nature. 400:590-593. http://dx.doi.org/10.1038/23072.
24. Moffitt, J.R., Y.R. Chemla, K. Aathavan, S. Grimes, P.J. Jardine, D.L. Anderson, and C. Bustamante. 2009. Intersubunit coordination in a homomeric ring ATPase. Nature. 457:446-450. http://dx.doi.org/ 10.1038/nature07637.
25. Nakanishi-Matsui, M., M. Sekiya, R.K. Nakamoto, and M. Futai. 2010. The mechanism of rotating proton pumping ATPases. Biochim. Biophys. Acta. 1797:1343-1352. http://dx.doi.org/10.1016/j.bbabio.2010.02.014.
26. Numata, N., T. Kon, T. Shima, K. Imamula, T. Mogami, R. Ohkura, K. Sutoh, and K. Sutoh. 2008. Molecular mechanism of force generation by dynein, a molecular motor belonging to the AAA+ family. Biochem. Soc. Trans. 36:131-135. http://dx.doi.org/10.1042/BST0360131.
27. Oke, O.A., S.A. Burgess, E. Forgacs, P.J. Knight, T. Sakamoto, J.R. Sellers, H. White, and J. Trinick. 2010. Influence of lever structure on myosin 5a walking. Proc. Natl. Acad. Sci. USA. 107:2509-2514. http://dx.doi.org/10.1073/pnas.0906907107.
28. Okuno, D., R. Iino, and H. Noji. 2011. Rotation and structure of FoF1-ATP synthase. J. Biochem. 149:655-664. http://dx.doi.org/10.1093/ jb/mvr049.
29. Pardee, J.D., and J.A. Spudich. 1982. Purification of muscle actin. Methods Cell Biol. 24:271-289. http://dx.doi.org/10.1016/S0091-679X(08)60661-5.
30. Parker, D., Z. Bryant, and S.L. Delp. 2009. Coarse-grained structural modeling of molecular motors using multibody dynamics. Cell Mol Bioeng. 2:366-374. http://dx.doi.org/10.1007/s12195-009-0084-4.
31. Purcell, T.J., C. Morris, J.A. Spudich, and H.L. Sweeney. 2002. Role of the lever arm in the processive stepping of myosin V. Proc. Natl. Acad. Sci. USA. 99:14159-14164. http://dx.doi.org/10.1073/pnas.182539599.
32. Putkey, J.A., G.R. Slaughter, and A.R. Means. 1985. Bacterial expression and characterization of proteins derived from the chicken calmodulin cDNA and a calmodulin processed gene. J. Biol. Chem. 260:4704-4712.
33. Reck-Peterson, S.L., D.W. Provance Jr., M.S. Mooseker, and J.A. Mercer. 2000. Class V myosins. Biochim. Biophys. Acta. 1496:36-51. http://dx.doi.org/10.1016/S0167-4889(00)00007-0.
34. Rief, M., R.S. Rock, A.D. Mehta, M.S. Mooseker, R.E. Cheney, and J.A. Spudich. 2000. Myosin-V stepping kinetics: a molecular model for processivity. Proc. Natl. Acad. Sci. USA. 97:9482-9486. http://dx.doi.org/10.1073/pnas.97.17.9482.
35. Sakamoto, T., I. Amitani, E. Yokota, and T. Ando. 2000. Direct observation of processive movement by individual myosin V molecules. Biochem. Biophys. Res. Commun. 272:586-590. http:// dx.doi.org/10.1006/bbrc.2000.2819.
36. Sakamoto, T., A. Yildez, P.R. Selvin, and J.R. Sellers. 2005. Step-size is determined by neck length in myosin V. Biochemistry. 44:16203-16210. http://dx.doi.org/10.1021/bi0512086.
37. Schmeing, T.M., and V. Ramakrishnan. 2009. What recent ribosome structures have revealed about the mechanism of translation. Nature. 461:1234-1242. http://dx.doi.org/10.1038/nature08403.
38. Snyder, G.E., T. Sakamoto, J.A. Hammer III, J.R. Sellers, and P.R. Selvin. 2004. Nanometer localization of single green fluorescent proteins: evidence that myosin V walks hand-over-hand via telemark configuration. Biophys. J. 87:1776-1783. http://dx.doi.org/10.1529/biophysj.103.036897.
39. Sun, Y., and Y.E. Goldman. 2011. Lever-arm mechanics of processive myosins. Biophys. J. 101:1-11. http://dx.doi.org/10.1016/j.bpj.2011.05.026.
40. Sun, Y., H.W. Schroeder III, J.F. Beausang, K. Homma, M. Ikebe, and Y.E. Goldman. 2007. Myosin VI walks "wiggly" on actin with large and variable tilting. Mol. Cell. 28:954-964. http://dx.doi.org/10.1016/j.molcel.2007.10.029.
41. Sweeney, H.L., and A. Houdusse. 2010. Structural and functional insights into the myosin motor mechanism. Annu Rev Biophys. 39:539-557. http://dx.doi.org/10.1146/annurev.biophys.050708.133751.
42. Syed, S., G.E. Snyder, C. Franzini-Armstrong, P.R. Selvin, and Y.E. Goldman. 2006. Adaptability of myosin V studied by simultaneous detection of position and orientation. EMBO J. 25:1795-1803. http://dx.doi.org/10.1038/sj.emboj.7601060.
43. Terrak, M., G. Rebowski, R.C. Lu, Z. Grabarek, and R. Dominguez. 2005. Structure of the light chain-binding domain of myosin V. Proc. Natl. Acad. Sci. USA. 102:12718-12723. http://dx.doi.org/ 10.1073/pnas.0503899102.
44. Toprak, E., J. Enderlein, S. Syed, S.A. McKinney, R.G. Petschek, T. Ha, Y.E. Goldman, and P.R. Selvin. 2006. Defocused orientation and position imaging (DOPI) of myosin V. Proc. Natl. Acad. Sci. USA. 103:6495-6499. http://dx.doi.org/10.1073/pnas.0507134103.
45. Trybus, K.M., M.I. Gushchin, H. Lui, L. Hazelwood, E.B. Krementsova, N. Volkmann, and D. Hanein. 2007. Effect of calcium on calmodulin bound to the IQ motifs of myosin V. J. Biol. Chem. 282:23316-23325. http://dx.doi.org/10.1074/jbc.M701636200.
46. Veigel, C., F. Wang, M.L. Bartoo, J.R. Sellers, and J.E. Molloy. 2002. The gated gait of the processive molecular motor, myosin V. Nat. Cell Biol. 4:59-65. http://dx.doi.org/10.1038/ncb732.
47. Vilfan, A. 2005a. Elastic lever-arm model for myosin V. Biophys. J. 88:3792-3805. http://dx.doi.org/10.1529/biophysj.104.046763.
48. Vilfan, A. 2005b. Influence of fluctuations in actin structure on myosin V step size. J. Chem. Inf. Model. 45:1672-1675. http://dx.doi.org/10.1021/ci050182m.
49. Walker, M.L., S.A. Burgess, J.R. Sellers, F. Wang, J.A. Hammer III, J. Trinick, and P.J. Knight. 2000. Two-headed binding of a processive myosin to F-actin. Nature. 405:804-807. http://dx.doi.org/ 10.1038/35015592.